Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-15T23:26:13.717Z Has data issue: false hasContentIssue false
  • English
  • Français

Plasmodium prevalence across avian host species is positively associated with exposure to mosquito vectors

Published online by Cambridge University Press:  23 September 2015

MATTHEW C. I. MEDEIROS ,
ROBERT E. RICKLEFS ,
JEFFREY D. BRAWN  and
GABRIEL L. HAMER
MATTHEW C. I. MEDEIROS*
Affiliation:
Department of Biology, University of Missouri-St. Louis, One University Boulevard, St. Louis, Missouri 63121-4499, USA Department of Entomology, Texas A&M University, College Station, Texas 77843-2475, USA
ROBERT E. RICKLEFS
Affiliation:
Department of Biology, University of Missouri-St. Louis, One University Boulevard, St. Louis, Missouri 63121-4499, USA
JEFFREY D. BRAWN
Affiliation:
Department of Natural Resources and Environmental Sciences, University of Illinois, 1102 South Goodwin Ave., Urbana, Illinois 61801, USA
GABRIEL L. HAMER
Affiliation:
Department of Entomology, Texas A&M University, College Station, Texas 77843-2475, USA
*
*Corresponding author. Department of Entomology, Texas A&M University, College Station, Texas 77843-2475, USA. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The prevalence of vector-borne parasites varies greatly across host species, and this heterogeneity has been used to relate infectious disease susceptibility to host species traits. However, a few empirical studies have directly associated vector-borne parasite prevalence with exposure to vectors across hosts. Here, we use DNA sequencing of blood meals to estimate utilization of different avian host species by Culex mosquitoes, and relate utilization by these malaria vectors to avian Plasmodium prevalence. We found that avian host species that are highly utilized as hosts by avian malaria vectors are significantly more likely to have Plasmodium infections. However, the effect was not consistent among individual Plasmodium taxa. Exposure to vector bites may therefore influence the relative number of all avian Plasmodium infections among host species, while other processes, such as parasite competition and host-parasite coevolution, delimit the host distributions of individual Plasmodium species. We demonstrate that links between avian malaria susceptibility and host traits can be conditioned by patterns of exposure to vectors. Linking vector utilization rates to host traits may be a key area of future research to understand mechanisms that produce variation in the prevalence of vector-borne pathogens among host species.

Keywords

Avian malaria parasitesmalaria vectorshost–vector interactionsmosquito feeding patternsPlasmodium
Type
Research Article
Information
Parasitology , Volume 142 , Issue 13 , November 2015 , pp. 1612 - 1620
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Boakye, D. A., Tang, J., Truc, P., Merriweather, A. and Unnasch, T. R. (1999). Identification of bloodmeals in haematophagous Diptera by cytochrome B heteroduplex analysis. Medical and Veterinary Entomology 13, 282–287.CrossRefGoogle ScholarPubMed
Carlson, J. S., Walther, E., TroutFryxell, R., Staley, S., Tell, L. A., Sehgal, R. N., Barker, C. M., and Cornel, A. J. (2015). Identifying avian malaria vectors: sampling methods influence outcomes. Parasites and Vectors 8, 1–16.CrossRefGoogle ScholarPubMed
Charlwood, J. D., Smith, T., Lyimo, E., Kitua, A. Y., Masanja, H., Booth, M., Alonso, P. L. and Tanner, M. (1998). Incidence of Plasmodium falciparum infection in infants in relation to exposure to sporozoite-infected anophelines. American Journal of Tropical Medicine and Hygiene 59, 243–251.CrossRefGoogle ScholarPubMed
Chaves, L. F., Hamer, G. L., Walker, E. D., Brown, W. M., Ruiz, M. O. and Kitron, U. D. (2011). Climatic variability and landscape heterogeneity impact urban mosquito diversity and vector abundance and infection. Ecosphere 2, art70.CrossRefGoogle Scholar
Cornet, S., Nicot, A., Rivero, A. and Gandon, S. (2013). Malaria infection increases bird attractiveness to uninfected mosquitoes. Ecology Letters 16, 323–329.CrossRefGoogle ScholarPubMed
Crabtree, M. B., Savage, H. M. and Miller, B. R. (1995). Development of a species-diagnostic polymerase chain reaction assay for the identification of Culex vectors of St. Louis encephalitis virus based on interspecies sequence variation in ribosomal DNA spacers. American Journal of Tropical Medicine and Hygiene 53, 105–109.CrossRefGoogle ScholarPubMed
Cupp, E. W., Zhang, D., Yue, X., Cupp, M. S., Guyer, C., Sprenger, T. R. and Unnasch, T. R. (2004). Identification of reptilian and amphibian blood meals from mosquitoes in an eastern equine encephalomyelitis virus focus in central Alabama. American Journal of Tropical Medicine and Hygiene 71, 272–276.CrossRefGoogle Scholar
Fallon, S. M., Bermingham, E. and Ricklefs, R. E. (2003 a). Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57, 606–615.Google ScholarPubMed
Fallon, S. M., Ricklefs, R. E., Swanson, B. L. and Bermingham, E. (2003 b). Detecting avian malaria: an improved polymerase chain reaction diagnostic. Journal of Parasitology 89, 1044–1047.CrossRefGoogle ScholarPubMed
Fallon, S. M., Bermingham, E. and Ricklefs, R. E. (2005). Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. American Naturalist 165, 466–480.CrossRefGoogle ScholarPubMed
Fecchio, A., Lima, M. R., Silveira, P., Braga, É. M. and Marini, M. Â. (2011). High prevalence of blood parasites in social birds from a Neotropical savanna in Brazil. Emu 111, 132–138.CrossRefGoogle Scholar
Fecchio, A., Lima, M. R., Svensson-Coelho, M., Marini, M. Â. and Ricklefs, R. E. (2013). Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. Parasitology 140, 181–192.CrossRefGoogle Scholar
Gager, A. B., Del Rosario Loaiza, J., Dearborn, D. C. and Bermingham, E. (2008). Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host? Molecular Ecology 17, 2552–2561.CrossRefGoogle Scholar
Garvin, M. C. and Remsen, J. V. (1997). An alternative hypothesis for heavier parasite loads of brightly colored birds: exposure at the nest. Auk 114, 179–191.Google Scholar
González, A. D., Matta, N. E., Ellis, V. A., Miller, E. T., Ricklefs, R. E. and Gutiérrez, H. R. (2014). Mixed species flock, nest height, and elevation partially explain avian haemoparasite prevalence in Colombia. PLoS ONE 9, e100695.CrossRefGoogle ScholarPubMed
Hamer, G. L., Kitron, U. D., Goldberg, T. L., Brawn, J. D., Loss, S. R., Ruiz, M. O., Hayes, D. B. and Walker, E. D. (2009). Host selection by Culex pipiens mosquitoes and West Nile virus amplification. American Journal of Tropical Medicine and Hygiene 80, 268–278.CrossRefGoogle ScholarPubMed
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.CrossRefGoogle Scholar
Hellgren, O., Bensch, S. and Malmqvist, B. (2008). Bird hosts, blood parasites and their vectors–associations uncovered by molecular analyses of blackfly blood meals. Molecular Ecology 17, 1605–1613.CrossRefGoogle ScholarPubMed
Ivanova, N. V., Zemlak, T. S., Hanner, R. H. and Hebert, P. D. (2007). Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes 7, 544–548.CrossRefGoogle Scholar
Kent, R. J. (2009 a). Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Molecular Ecology Resources 9, 4–18.CrossRefGoogle Scholar
Kent, R. J., Juliusson, L., Weissmann, M., Evans, S. and Komar, N. (2009 b). Seasonal blood-feeding behavior of Culex tarsalis (Diptera: Culicidae) in Weld county, Colorado, 2007. Journal of Medical Entomology 46, 380–390.CrossRefGoogle ScholarPubMed
Kilpatrick, A. M., Daszak, P., Jones, M. J., Marra, P. P. and Kramer, L. D. (2006). Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society of London B 273, 2327–2333.Google ScholarPubMed
Kimura, M., Darbro, J. M. and Harrington, L. C. (2010). Avian malaria parasites share congeneric mosquito vectors. Journal of Parasitology 96, 144–151.CrossRefGoogle ScholarPubMed
Krama, T., Krams, R., Cīrule, D., Moore, F. R., Rantala, M. J. and Krams, I. A. (2015). Intensity of haemosporidian infection of parids positively correlates with proximity to water bodies, but negatively with host survival. Journal of Ornithology 156(4). doi: 10.1007/s10336-015-1206-5.CrossRefGoogle Scholar
Krebs, B. L., Anderson, T. K., Goldberg, T. L., Hamer, G. L., Kitron, U. D., Newman, C. M., Ruiz, M. O., Walker, E. D. and Brawn, J. D. (2014). Host social behavior decreases exposure to vector-borne disease: a field experiment in a ‘hotspot’ of West Nile virus transmission. Proceedings of the Royal Society Series B 281, 20141586.Google Scholar
Lalubin, F., Bize, P., van Rooyen, J., Christe, P. and Glaizot, O. (2012). Potential evidence of parasite avoidance in an avian malarial vector. Animal Behaviour 84, 539–545.CrossRefGoogle Scholar
Latta, S. C. and Ricklefs, R. E. (2010). Prevalence patterns of avian haemosporida on Hispaniola. Journal of Avian Biology 41, 25–33.CrossRefGoogle Scholar
Loss, S. R., Hamer, G. L., Walker, E. D., Ruiz, M. O., Goldberg, T. L., Kitron, U. D. and Brawn, J. D. (2009). Avian host community structure and prevalence of West Nile virus in Chicago, Illinois. Oecologia 159, 415–424.CrossRefGoogle ScholarPubMed
Lutz, H. L., Hochachka, W. M., Engel, J. I., Bell, J. A., Tkach, V. V., Bates, J. M., Hackett, S. J. and Weckstein, J. D. (2015). Parasite prevalence corresponds to host life history in a diverse assemblage of Afrotropical birds and haemosporidian parasites. PLoS ONE 10, e0128851.Google Scholar
Macdonald, G. (1957). The Epidemiology and Control of Malaria. Oxford University Press, London, UK.Google Scholar
Martínez-de la Puente, J., Martínez, J., Rivero-de-Aguilar, J., Del Cerro, S. and Merino, S. (2013). Vector abundance determines Trypanosoma prevalence in nestling blue tits. Parasitology 140, 1009–1015.CrossRefGoogle ScholarPubMed
Medeiros, M. C. I., Hamer, G. L. and Ricklefs, R. E. (2013). Host compatibility rather than vector-host-encounter rate determines the host range of avian Plasmodium parasites. Proceedings of the Royal Society of London B 280, 20122947.Google ScholarPubMed
Medeiros, M. C. I., Ellis, V. A. and Ricklefs, R. E. (2014). Specialized avian Haemosporida trade reduced host breadth for increased prevalence. Journal of Evolutionary Biology 27, 2520–2528.CrossRefGoogle ScholarPubMed
Mendes, L., Piersma, T., Lecoq, M., Spaans, B. and Ricklefs, R. E. (2005). Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109, 396–404.CrossRefGoogle Scholar
Nevill, C. G., Some, E. S., Mung'ala, V. O., Mutemi, W., New, L., Marsh, K., Lengeler, C. and Snow, R. W. (1996). Insecticide-treated bednets reduce mortality and severe morbidity from malaria among children on the Kenyan coast. Tropical Medicine and International Health 1, 139–146.CrossRefGoogle ScholarPubMed
Nunn, C. L. and Heymann, E. W. (2005). Malaria infection and host behavior: a comparative study of Neotropical primates. Behavioral Ecology and Sociobiology 59, 30–37.CrossRefGoogle Scholar
Nunn, C. L., Gittleman, J. L. and Antonovics, J. (2000). Promiscuity and the primate immune system. Science 290, 1168–1170.CrossRefGoogle ScholarPubMed
Poulin, R. (2011). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.Google Scholar
Ricklefs, R. E. (1992). Embryonic development period and the prevalence of avian blood parasites. Proceedings of the National Academy of Sciences 89, 4722–4725.CrossRefGoogle ScholarPubMed
Ricklefs, R. E., Swanson, B. L., Fallon, S. M., Martinez-Abrain, A., Scheuerlein, A., Gray, J. and Latta, S. C. (2005). Community relationships of avian malaria parasites in southern Missouri. Ecological Monographs 75, 543–559.CrossRefGoogle Scholar
Ross, R. (1911). The Prevention of Malaria. E.P. Dutton & Company, New York, USA.Google ScholarPubMed
Scheuerlein, A. and Ricklefs, R. E. (2004). Prevalence of blood parasites in European passeriform birds. Proceedings of the Royal Society of London B 271, 1363–1370.CrossRefGoogle ScholarPubMed
Snow, R. W., Lindsay, S. W., Hayes, R. J. and Greenwood, B. M. (1988). Permethrin-treated bed nets (mosquito nets) prevent malaria in Gambian children. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 838–842.CrossRefGoogle ScholarPubMed
Super, P. E. and van Riper, C. III (1995). A comparison of avian hematozoan epizootiology in two California coastal scrub communities. Journal of Wildlife Diseases 31, 447–461.CrossRefGoogle ScholarPubMed
Svensson-Coelho, M., Blake, J. G., Loiselle, B. A., Penrose, A. S., Parker, P. G. and Ricklefs, R. E. (2013). Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a western Amazon assemblage. Ornithological Monographs 2013, 1–47.CrossRefGoogle Scholar
Tella, J. L., Blanco, G., Forero, M. G., Gajón, Á., Donázar, J. A. and Hiraldo, F. (1999). Habitat, world geographic range, and embryonic development of hosts explain the prevalence of avian hematozoa at small spatial and phylogenetic scales. Proceedings of the National Academy of Sciences 96, 1785–1789.CrossRefGoogle ScholarPubMed
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
van Riper, C. III, van Riper, S. G., Goff, M. L. and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327–344.CrossRefGoogle Scholar